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Molecular interactions of brown marmorated stink bug, Halyomorpha halys with its bacterial endosymbiont, Pantoea carbekii and their role in nutrient provisioning

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2018, Doctor of Philosophy, Ohio State University, Entomology.
Phytophagous insects of Hemiptera exclusively feed on the plant sap and cause severe yield loss to many important agricultural commodities. Since the last decade, there has been a significant increase in application of targeted insecticides to manage these hemipteran pests. Halyomorpha halys, (brown marmorated stink bug, BMSB) is a notorious, polyphagous Hemipteran pest that causes severe feeding damage to more than 100 agricultural and ornamental plants. Since its invasion in 1996, it has spread to 44 states in the U.S. and four Canadian provinces. Soybean (Glycine max) is one of the major agricultural crops in U.S. and BMSB causes severe injury to reproductive tissues resulting in a significant yield loss. BMSB feeds on the plant sap that is nutritionally imbalanced; however, some nutrients are potentially provided by its bacterial endosymbiont, Pantoea carbekii. My research focused on feeding preferences and damage caused to soybean by BMSB and also investigated the molecular coordination of the BMSB-P. carbekii association. Specialty soybean is a major focus for Ohio, and there are several varieties of soybean grown as dietary staple for human and animal feed. I was interested to test for any preference of BMSB on these varieties. BMSB caused severe feeding damage all soybean varieties and no feeding preference was observed among soybean varieties. There was a significant negative impact on the seed weight and damage incidence of all soybean varieties. Results suggested that scouting should be intensified during soybean growth stages that are susceptible to BMSB infestation and should be treated similar to conventional soybean if the infestation exceeds the economic threshold. Chapter three revealed the importance of P450 enzymes belonging to the CYP6 sub-family that are well known for detoxification and metabolism of plant secondary metabolites encountered in the diet of many generalist insects. I characterized and analyzed the expression of three HhCYP6 genes in different tissues, sexes and when BMSB was exposed to different diets. The results showed differential expression of HhCYP6 genes in tissues suggesting their role in diverse and important physiological functions related to the gut, fat body and Malpighian tubules. To further study the functions of genes potentially important to BMSB, I have successfully developed an RNAi injection technique in chapter 4. The gene expression of three BMSB target genes (cytochrome P450 reductase (HhCPR), catalase (HhCAT) and vacuolar-type ATPase (HhvATP)) was significantly decreased. In addition, knocking down the expression of HhvATP negatively impacted the survival of BMSB. Establishing a standard method of dsRNA delivery via microinjection in BMSB will help in documenting essential functions of several important candidate genes. Chapters five and six revealed the importance of the BMSB-P. carbekii interaction, providing insights on the molecular and physiological functions as well as the nutrient provisioning role of P. carbekii. Chapter 5 determined the impact of P. carbekii on free amino acid abundance in BMSB. The absence of P. carbekii resulted in significant decrease in the essential and non-essential amino acid concentrations, except for lysine and alanine, which were significantly higher in aposymbiotic BMSB. By sequencing metatranscriptomes in chapter six, we characterized the interactions between BMSB and P. carbekii that help in the biosynthesis of several nutrients. Results from both metabolomic and metatranscriptomic studies provide insights on molecular and physiological collaborations of BMSB and P. carbekii in biosynthesis and metabolism of nutrients including amino acids. A total of 9 BMSB transcripts from the metatranscriptome differentially expressed among symbiotic and aposymbiotic BMSB, including D-aspartate oxidase, succcinylornithine/ acetylornithine transaminase, thiazole synthase and two proteins (histone H3 and protein pelota). The findings of chapter six suggested that the association of P. carbekii with BMSB is essential in the synthesis of nutrients such as arginine, lysine and thiamine. The information on differentially expressed genes in this study can be exploited to target specific genes/enzymes that affect the BMSB-P. carbekii association and potentially help in developing novel pest management strategies. To conclude, my research revealed the basic biology of BMSB, also molecular and physiological coordination of BMSB-P. carbekii association. Results from this work contributed to the fundamental biology and molecular physiology of insect-symbiont interactions that sheds light on detoxification and nutrient providing mechanisms. Successful use of RNAi to target differentially expressed genes that affect the BMSB-P. carbekii association may provide possible RNAi-based pest management.
Andrew Michel (Advisor)
Peter Piermarini (Committee Member)
Zakee Sabree (Committee Member)
David Denlinger (Committee Member)
253 p.

Recommended Citations

Citations

  • Mittapelly, P. (2018). Molecular interactions of brown marmorated stink bug, Halyomorpha halys with its bacterial endosymbiont, Pantoea carbekii and their role in nutrient provisioning [Doctoral dissertation, Ohio State University]. OhioLINK Electronic Theses and Dissertations Center. http://rave.ohiolink.edu/etdc/view?acc_num=osu1543246781490262

    APA Style (7th edition)

  • Mittapelly, Priyanka. Molecular interactions of brown marmorated stink bug, Halyomorpha halys with its bacterial endosymbiont, Pantoea carbekii and their role in nutrient provisioning. 2018. Ohio State University, Doctoral dissertation. OhioLINK Electronic Theses and Dissertations Center, http://rave.ohiolink.edu/etdc/view?acc_num=osu1543246781490262.

    MLA Style (8th edition)

  • Mittapelly, Priyanka. "Molecular interactions of brown marmorated stink bug, Halyomorpha halys with its bacterial endosymbiont, Pantoea carbekii and their role in nutrient provisioning." Doctoral dissertation, Ohio State University, 2018. http://rave.ohiolink.edu/etdc/view?acc_num=osu1543246781490262

    Chicago Manual of Style (17th edition)